1932

Abstract

This review examines the impact of microbial communities colonizing food processing environments in the form of biofilms on food safety and food quality. The focus is both on biofilms formed by pathogenic and spoilage microorganisms and on those formed by harmless or beneficial microbes, which are of particular relevance in the processing of fermented foods. Information is presented on intraspecies variability in biofilm formation, interspecies relationships of cooperativism or competition within biofilms, the factors influencing biofilm ecology and architecture, and how these factors may influence removal. The effect on the biofilm formation ability of particular food components and different environmental conditions that commonly prevail during food processing is discussed. Available tools for the in situ monitoring and characterization of wild microbial biofilms in food processing facilities are explored. Finally, research on novel agents or strategies for the control of biofilm formation or removal is summarized.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-food-032818-121805
2019-03-25
2024-10-04
Loading full text...

Full text loading...

/deliver/fulltext/food/10/1/annurev-food-032818-121805.html?itemId=/content/journals/10.1146/annurev-food-032818-121805&mimeType=html&fmt=ahah

Literature Cited

  1. Al-Seraih A, Belguesmia Y, Baah J, Szunerits S, Boukherroub R, Drider D 2017. Enterocin B3A-B3B produced by LAB collected from infant faeces: potential utilization in the food industry for Listeria monocytogenes biofilm management. Antonie Van Leeuwenhoek 110:2205–19
    [Google Scholar]
  2. Álvarez-Ordóñez A, Alvseike O, Omer MK, Heir E, Axelsson L et al. 2013. Heterogeneity in resistance to food-related stresses and biofilm formation ability among verocytotoxigenic Escherichia coli strains. Int. J. Food Microbiol. 161:3220–30
    [Google Scholar]
  3. Anand S, Singh D 2013. Resistance of the constitutive microflora of biofilms formed on whey reverse-osmosis membranes to individual cleaning steps of a typical clean-in-place protocol. J. Dairy Sci. 96:106213–22
    [Google Scholar]
  4. Araújo PA, Machado I, Meireles A, Leiknes T, Mergulhão F et al. 2017. Combination of selected enzymes with cetyltrimethylammonium bromide in biofilm inactivation, removal and regrowth. Food Res. Int. 95:101–7
    [Google Scholar]
  5. Ashraf MA, Ullah S, Ahmad I, Qureshi AK, Balkhair KS, Abdur Rehman M 2014. Green biocides, a promising technology: current and future applications to industry and industrial processes. J. Sci. Food Agric. 94:3388–403
    [Google Scholar]
  6. Axelsson L, Holck A, Rud I, Samah D, Tierce P et al. 2013. Cleaning of conveyor belt materials using ultrasound in a thin layer of water. J. Food Prot. 76:81401–7
    [Google Scholar]
  7. Balsa-Canto E, Vilas C, López-Núñez A, Mosquera-Fernández M, Briandet R et al. 2017. Modeling reveals the role of aging and glucose uptake impairment in L1A1 Listeria monocytogenes biofilm life cycle. Front. Microbiol. 8:2118
    [Google Scholar]
  8. Ban G-H, Kang D-H 2016. Effect of sanitizer combined with steam heating on the inactivation of foodborne pathogens in a biofilm on stainless steel. Food Microbiol 55:47–54
    [Google Scholar]
  9. Bas S, Kramer M, Stopar D 2017. Biofilm surface density determines biocide effectiveness. Front. Microbiol. 8:2443
    [Google Scholar]
  10. Bassi D, Cappa F, Gazzola S, Orrù L, Cocconcelli PS 2017. Biofilm formation on stainless steel by Streptococcus thermophilus UC8547 in milk environments is mediated by the proteinase PrtS. Appl. Environ. Microbiol. 83:8e02840–16
    [Google Scholar]
  11. Ben-Ishay N, Oknin H, Steinberg D, Berkovich Z, Reifen R, Shemesh M 2017. Enrichment of milk with magnesium provides healthier and safer dairy products. npj Biofilms Microbiomes 3:124
    [Google Scholar]
  12. Benítez-Cabello A, Romero-Gil V, Rodríguez-Gómez F, Garrido-Fernández A, Jiménez-Díaz R, Arroyo-López FN 2015. Evaluation and identification of poly-microbial biofilms on natural green Gordal table olives. Antonie Van Leeuwenhoek 108:3597–610
    [Google Scholar]
  13. Benítez-Páez A, Sanz Y 2017. Multi-locus and long amplicon sequencing approach to study microbial diversity at species level using the MinIONTM portable nanopore sequencer. Gigascience 6:71–12
    [Google Scholar]
  14. Berlanga M, Guerrero R 2016. Living together in biofilms: the microbial cell factory and its biotechnological implications. Microb. Cell Fact. 15:1165
    [Google Scholar]
  15. Bolocan AS, Pennone V, O'Connor PM, Coffey A, Nicolau AI et al. 2017. Inhibition of Listeria monocytogenes biofilms by bacteriocin-producing bacteria isolated from mushroom substrate. J. Appl. Microbiol. 122:1279–93
    [Google Scholar]
  16. Branck TA, Hurley MJ, Prata GN, Crivello CA, Marek PJ 2017. Efficacy of a sonicating swab for removal and capture of Listeria monocytogenes in biofilms on stainless steel. Appl. Environ. Microbiol. 83:11e00109–17
    [Google Scholar]
  17. Brauge T, Faille C, Sadovskaya I, Charbit A, Benezech T et al. 2018. The absence of N-acetylglucosamine in wall teichoic acids of Listeria monocytogenes modifies biofilm architecture and tolerance to rinsing and cleaning procedures. PLOS ONE 13:1e0190879
    [Google Scholar]
  18. Bridier A, Sanchez-Vizuete P, Guilbaud M, Piard J-C, Naïtali M, Briandet R 2015. Biofilm-associated persistence of food-borne pathogens. Food Microbiol 45:Pt. B167–78
    [Google Scholar]
  19. Brown HL, Hanman K, Reuter M, Betts RP, van Vliet AHM 2015. Campylobacter jejuni biofilms contain extracellular DNA and are sensitive to DNase I treatment. Front. Microbiol. 6:699
    [Google Scholar]
  20. Brown HL, Reuter M, Salt LJ, Cross KL, Betts RP, van Vliet AHM 2014. Chicken juice enhances surface attachment and biofilm formation of Campylobacter jejuni. Appl. Environ. Microbiol. 80:227053–60
    [Google Scholar]
  21. Bruchmann J, Sachsenheimer K, Rapp BE, Schwartz T 2015. Multi-channel microfluidic biosensor platform applied for online monitoring and screening of biofilm formation and activity. PLOS ONE 10:2e0117300
    [Google Scholar]
  22. Buzón-Durán L, Alonso-Calleja C, Riesco-Peláez F, Capita R 2017. Effect of sub-inhibitory concentrations of biocides on the architecture and viability of MRSA biofilms. Food Microbiol 65:294–301
    [Google Scholar]
  23. Caballero Gómez N, Abriouel H, Grande MJ, Pérez Pulido R, Gálvez A 2013. Combined treatments of enterocin AS-48 with biocides to improve the inactivation of methicillin-sensitive and methicillin-resistant Staphylococcus aureus planktonic and sessile cells. Int. J. Food Microbiol. 163:2–396–100
    [Google Scholar]
  24. Capita R, Buzón-Durán L, Riesco-Peláez F, Alonso-Calleja C 2017. Effect of sub-lethal concentrations of biocides on the structural parameters and viability of the biofilms formed by Salmonella Typhimurium. Foodborne Pathog. Dis. 14:6350–56
    [Google Scholar]
  25. Capita R, Riesco-Peláez F, Alonso-Hernando A, Alonso-Calleja C 2014. Exposure of Escherichia coli ATCC 12806 to sublethal concentrations of food-grade biocides influences its ability to form biofilm, resistance to antimicrobials, and ultrastructure. Appl. Environ. Microbiol. 80:41268–80
    [Google Scholar]
  26. Carpino S, Randazzo CL, Pino A, Russo N, Rapisarda T et al. 2017. Influence of PDO Ragusano cheese biofilm microbiota on flavour compounds formation. Food Microbiol 61:126–35
    [Google Scholar]
  27. Chaitiemwong N, Hazeleger WC, Beumer RR 2014. Inactivation of Listeria monocytogenes by disinfectants and bacteriophages in suspension and stainless steel carrier tests. J. Food Prot. 77:122012–20
    [Google Scholar]
  28. Chakravorty S, Bhattacharya S, Chatzinotas A, Chakraborty W, Bhattacharya D, Gachhui R 2016. Kombucha tea fermentation: microbial and biochemical dynamics. Int. J. Food Microbiol. 220:63–72
    [Google Scholar]
  29. Chamberland J, Lessard M-H, Doyen A, Labrie S, Pouliot Y 2017. Biofouling of ultrafiltration membrane by dairy fluids: characterization of pioneer colonizer bacteria using a DNA metabarcoding approach. J. Dairy Sci. 100:2981–90
    [Google Scholar]
  30. Chen C-Y, Hofmann CS, Cottrell BJ, Strobaugh TP Jr., Paoli GC et al. 2013. Phenotypic and genotypic characterization of biofilm forming capabilities in non-O157 Shiga toxin-producing Escherichia coli strains. PLOS ONE 8:12e84863
    [Google Scholar]
  31. Cherifi T, Jacques M, Quessy S, Fravalo P 2017. Impact of nutrient restriction on the structure of Listeria monocytogenes biofilm grown in a microfluidic system. Front. Microbiol. 8:864
    [Google Scholar]
  32. Chopra L, Singh G, Kumar Jena K, Sahoo DK 2015. Sonorensin: a new bacteriocin with potential of an anti-biofilm agent and a food biopreservative. Sci. Rep. 5:113412
    [Google Scholar]
  33. Chylkova T, Cadena M, Ferreiro A, Pitesky M 2017. Susceptibility of Salmonella biofilm and planktonic bacteria to common disinfectant agents used in poultry processing. J. Food Prot. 80:71072–79
    [Google Scholar]
  34. Corcoran M, Morris D, De Lappe N, O'Connor J, Lalor P et al. 2014. Commonly used disinfectants fail to eradicate Salmonella enterica biofilms from food contact surface materials. Appl. Environ. Microbiol. 80:41507–14
    [Google Scholar]
  35. Coronel-León J, Marqués AM, Bastida J, Manresa A 2016. Optimizing the production of the biosurfactant lichenysin and its application in biofilm control. J. Appl. Microbiol. 120:199–111
    [Google Scholar]
  36. Cossu A, Si Y, Sun G, Nitin N 2017. Antibiofilm effect of poly(vinyl alcohol–coethylene) halamine film against Listeria innocua and Escherichia coli O157:H7. Appl. Environ. Microbiol. 83:19e00975–17
    [Google Scholar]
  37. Coughlan LM, Cotter PD, Hill C, Alvarez-Ordóñez A 2016. New weapons to fight old enemies: novel strategies for the (bio)control of bacterial biofilms in the food industry. Front. Microbiol. 7:1641
    [Google Scholar]
  38. Cruciata M, Gaglio R, Scatassa ML, Sala G, Cardamone C et al. 2017. Formation and characterization of early bacterial biofilms on different wood typologies applied in dairy production. Appl. Environ. Microbiol. 84:4e02107–17
    [Google Scholar]
  39. Daneshvar Alavi HE, Truelstrup Hansen L 2013. Kinetics of biofilm formation and desiccation survival of Listeria monocytogenes in single and dual species biofilms with Pseudomonas fluorescens, Serratia proteamaculans or Shewanella baltica on food-grade stainless steel surfaces. Biofouling 29:101253–68
    [Google Scholar]
  40. da Silva Fernandes M, Kabuki DY, Kuaye AY 2015. Behavior of Listeria monocytogenes in a multi-species biofilm with Enterococcus faecalis and Enterococcus faecium and control through sanitation procedures. Int. J. Food Microbiol. 200:5–12
    [Google Scholar]
  41. Dhowlaghar N, De Abrew Abeysundara P, Nannapaneni R, Schilling MW, Chang S et al. 2018. Biofilm formation by Salmonella spp. in catfish mucus extract under industrial conditions. Food Microbiol 70:172–80
    [Google Scholar]
  42. Dimakopoulou-Papazoglou D, Lianou A, Koutsoumanis KP 2016. Modelling biofilm formation of Salmonella enterica ser. Newport as a function of pH and water activity. Food Microbiol 53:Pt. B76–81
    [Google Scholar]
  43. Doijad SP, Barbuddhe SB, Garg S, Poharkar KV, Kalorey DR et al. 2015. Biofilm-forming abilities of Listeria monocytogenes serotypes isolated from different sources. PLOS ONE 10:9e0137046
    [Google Scholar]
  44. Duanis-Assaf D, Steinberg D, Chai Y, Shemesh M 2016. The LuxS based quorum sensing governs lactose induced biofilm formation by Bacillus subtilis. Front. Microbiol. 6:1517
    [Google Scholar]
  45. Dubois-Brissonnet F, Trotier E, Briandet R 2016. The biofilm lifestyle involves an increase in bacterial membrane saturated fatty acids. Front. Microbiol. 7:1673
    [Google Scholar]
  46. Dzieciol M, Schornsteiner E, Muhterem-Uyar M, Stessl B, Wagner M, Schmitz-Esser S 2016. Bacterial diversity of floor drain biofilms and drain waters in a Listeria monocytogenes contaminated food processing environment. Int. J. Food Microbiol. 223:33–40
    [Google Scholar]
  47. Endersen L, Buttimer C, Nevin E, Coffey A, Neve H et al. 2017. Investigating the biocontrol and anti-biofilm potential of a three phage cocktail against Cronobacter sakazakii in different brands of infant formula. Int. J. Food Microbiol. 253:1–11
    [Google Scholar]
  48. Fagerlund A, Langsrud S, Heir E, Mikkelsen MI, Møretrø T 2016. Biofilm matrix composition affects the susceptibility of food associated staphylococci to cleaning and disinfection agents. Front. Microbiol. 7:856
    [Google Scholar]
  49. Fagerlund A, Møretrø T, Heir E, Briandet R, Langsrud S 2017. Cleaning and disinfection of biofilms composed of Listeria monocytogenes and background microbiota from meat processing surfaces. Appl. Environ. Microbiol. 83:17e01046–17
    [Google Scholar]
  50. Faille C, Bénézech T, Midelet-Bourdin G, Lequette Y, Clarisse M et al. 2014. Sporulation of Bacillus spp. within biofilms: a potential source of contamination in food processing environments. Food Microbiol 40:64–74
    [Google Scholar]
  51. Farhat NM, Staal M, Siddiqui A, Borisov SM, Bucs SS, Vrouwenvelder JS 2015. Early non-destructive biofouling detection and spatial distribution: application of oxygen sensing optodes. Water Res 83:10–20
    [Google Scholar]
  52. Feng G, Cheng Y, Wang S-Y, Borca-Tasciuc DA, Worobo RW, Moraru CI 2015. Bacterial attachment and biofilm formation on surfaces are reduced by small-diameter nanoscale pores: How small is small enough. npj Biofilms Microbiomes 1:115022
    [Google Scholar]
  53. Feng G, Cheng Y, Wang S-Y, Hsu LC, Feliz Y et al. 2014. Alumina surfaces with nanoscale topography reduce attachment and biofilm formation by Escherichia coli and Listeria spp. Biofouling 30:101253–68
    [Google Scholar]
  54. Fialho JF, Naves EA, Bernardes PC, Ferreira DC, dos Anjos LD et al. 2018. Stainless steel and polyethylene surfaces functionalized with silver nanoparticles. Food Sci. Technol. Int. 24:187–94
    [Google Scholar]
  55. Field D, O'Connor R, Cotter PD, Ross RP, Hill C 2016. In vitro activities of nisin and nisin derivatives alone and in combination with antibiotics against Staphylococcus biofilms. Front. Microbiol. 7:508
    [Google Scholar]
  56. Flemming H-C, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S 2016. Biofilms: an emergent form of bacterial life. Nat. Rev. Microbiol. 14:9563–75
    [Google Scholar]
  57. Fox EM, Solomon K, Moore JE, Wall PG, Fanning S 2014. Phylogenetic profiles of in-house microflora in drains at a food production facility: comparison and biocontrol implications of Listeria-positive and -negative bacterial populations. Appl. Environ. Microbiol. 80:113369–74
    [Google Scholar]
  58. Gaglio R, Cruciata M, Di Gerlando R, Scatassa ML, Cardamone C et al. 2016. Microbial activation of wooden vats used for traditional cheese production and evolution of neoformed biofilms. Appl. Environ. Microbiol. 82:2585–95
    [Google Scholar]
  59. Gião MS, Blanc S, Porta S, Belenguer J, Keevil CW 2015. Improved recovery of Listeria monocytogenes from stainless steel and polytetrafluoroethylene surfaces using air/water ablation. J. Appl. Microbiol. 119:1253–62
    [Google Scholar]
  60. Gião MS, Keevil CW 2014. Listeria monocytogenes can form biofilms in tap water and enter into the viable but non-cultivable state. Microb. Ecol. 67:3603–11
    [Google Scholar]
  61. Giaouris E, Chorianopoulos N, Doulgeraki A, Nychas G-J 2013. Co-culture with Listeria monocytogenes within a dual-species biofilm community strongly increases resistance of Pseudomonas putida to benzalkonium chloride. PLOS ONE 8:10e77276
    [Google Scholar]
  62. Giaouris E, Heir E, Desvaux M, Hébraud M, Møretrø T et al. 2015. Intra- and inter-species interactions within biofilms of important foodborne bacterial pathogens. Front. Microbiol. 6:841
    [Google Scholar]
  63. Gingichashvili S, Duanis-Assaf D, Shemesh M, Featherstone JDB, Feuerstein O, Steinberg D 2017. Bacillus subtilis biofilm development: a computerized study of morphology and kinetics. Front. Microbiol. 8:2072
    [Google Scholar]
  64. Gkana EN, Doulgeraki AI, Chorianopoulos NG, Nychas G-JE 2017. Anti-adhesion and anti-biofilm potential of organosilane nanoparticles against foodborne pathogens. Front. Microbiol. 8:1295
    [Google Scholar]
  65. Gomes LC, Deschamps J, Briandet R, Mergulhão FJ 2018. Impact of modified diamond-like carbon coatings on the spatial organization and disinfection of mixed-biofilms composed of Escherichia coli and Pantoea agglomerans industrial isolates. Int. J. Food Microbiol. 277:74–82
    [Google Scholar]
  66. González S, Fernández L, Campelo AB, Gutiérrez D, Martínez B et al. 2017. The behavior of Staphylococcus aureus dual-species biofilms treated with bacteriophage phiIPLA-RODI depends on the accompanying microorganism. Appl. Environ. Microbiol. 83:3e02821–16
    [Google Scholar]
  67. Grounta A, Doulgeraki AI, Panagou EZ 2015. Quantification and characterization of microbial biofilm community attached on the surface of fermentation vessels used in green table olive processing. Int. J. Food Microbiol. 203:41–48
    [Google Scholar]
  68. Guilbaud M, Piveteau P, Desvaux M, Brisse S, Briandet R 2015. Exploring the diversity of Listeria monocytogenes biofilm architecture by high-throughput confocal laser scanning microscopy and the predominance of the honeycomb-like morphotype. Appl. Environ. Microbiol. 81:51813–19
    [Google Scholar]
  69. Gutiérrez D, Rodríguez-Rubio L, Martínez B, Rodríguez A, García P 2016. Bacteriophages as weapons against bacterial biofilms in the food industry. Front. Microbiol. 7:825
    [Google Scholar]
  70. Gutiérrez D, Ruas-Madiedo P, Martínez B, Rodríguez A, García P 2014. Effective removal of staphylococcal biofilms by the endolysin LysH5. PLOS ONE 9:9e107307
    [Google Scholar]
  71. Han Q, Song X, Zhang Z, Fu J, Wang X et al. 2017. Removal of foodborne pathogen biofilms by acidic electrolyzed water. Front. Microbiol. 8:988
    [Google Scholar]
  72. Hayrapetyan H, Muller L, Tempelaars M, Abee T, Nierop Groot M 2015. Comparative analysis of biofilm formation by Bacillus cereus reference strains and undomesticated food isolates and the effect of free iron. Int. J. Food Microbiol. 200:72–79
    [Google Scholar]
  73. Heir E, Møretrø T, Simensen A, Langsrud S 2018. Listeria monocytogenes strains show large variations in competitive growth in mixed culture biofilms and suspensions with bacteria from food processing environments. Int. J. Food Microbiol. 275:46–55
    [Google Scholar]
  74. Herschend J, Damholt ZBV, Marquard AM, Svensson B, Sørensen SJ et al. 2017. A meta-proteomics approach to study the interspecies interactions affecting microbial biofilm development in a model community. Sci. Rep. 7:116483
    [Google Scholar]
  75. Hsu LC, Fang J, Borca-Tasciuc DA, Worobo RW, Moraru CI 2013. Effect of micro- and nanoscale topography on the adhesion of bacterial cells to solid surfaces. Appl. Environ. Microbiol. 79:82703–12
    [Google Scholar]
  76. Huang K, Chen J, Nugen SR, Goddard JM 2016.a Hybrid antifouling and antimicrobial coatings prepared by electroless co-deposition of fluoropolymer and cationic silica nanoparticles on stainless steel: efficacy against Listeria monocytogenes. ACS Appl. Mater. Interfaces. 8:2515926–36
    [Google Scholar]
  77. Huang K, McLandsborough LA, Goddard JM 2016.b Adhesion and removal kinetics of Bacillus cereus biofilms on Ni-PTFE modified stainless steel. Biofouling 32:5523–33
    [Google Scholar]
  78. Hussain MS, Kwon M, Tango CN, Oh DH 2018. Effect of electrolyzed water on the disinfection of Bacillus cereus biofilms: the mechanism of enhanced resistance of sessile cells in the biofilm matrix. J. Food Prot. 81:5860–69
    [Google Scholar]
  79. Hüwe C, Schmeichel J, Brodkorb F, Dohlen S, Kalbfleisch K et al. 2018. Potential of antimicrobial treatment of linear low-density polyethylene with poly((tert-butyl-amino)-methyl-styrene) to reduce biofilm formation in the food industry. Biofouling 34:4378–87
    [Google Scholar]
  80. Iliadis I, Daskalopoulou A, Simões M, Giaouris E 2018. Integrated combined effects of temperature, pH and sodium chloride concentration on biofilm formation by Salmonella enterica ser. Enteritidis and Typhimurium under low nutrient food-related conditions. Food Res. Int. 107:10–18
    [Google Scholar]
  81. Inaba T, Hori T, Aizawa H, Ogata A, Habe H 2017. Architecture, component, and microbiome of biofilm involved in the fouling of membrane bioreactors. npj Biofilms Microbiomes 3:15
    [Google Scholar]
  82. Inaba T, Hori T, Sato Y, Aoyagi T, Hanajima D et al. 2018. Eukaryotic microbiomes of membrane-attached biofilms in membrane bioreactors analyzed by high-throughput sequencing and microscopic observations. Microbes Environ 33:98–101
    [Google Scholar]
  83. Jahid IK, Lee N-Y, Kim A, Ha S-D 2013. Influence of glucose concentrations on biofilm formation, motility, exoprotease production, and quorum sensing in Aeromonas hydrophila. J. Food Prot 76:2239–47
    [Google Scholar]
  84. Jeon HR, Kwon MJ, Yoon KS 2018. Control of Listeria innocua biofilms on food contact surfaces with slightly acidic electrolyzed water and the risk of biofilm cells transfer to duck meat. J. Food Prot. 81:4582–92
    [Google Scholar]
  85. Jindal S, Anand S, Huang K, Goddard J, Metzger L, Amamcharla J 2016. Evaluation of modified stainless steel surfaces targeted to reduce biofilm formation by common milk sporeformers. J. Dairy Sci. 99:129502–13
    [Google Scholar]
  86. Jindal S, Anand S, Metzger L, Amamcharla J 2018. Short communication: a comparison of biofilm development on stainless steel and modified-surface plate heat exchangers during a 17-h milk pasteurization run. J. Dairy Sci. 101:42921–26
    [Google Scholar]
  87. Kadam SR, den Besten HMW, van der Veen S, Zwietering MH, Moezelaar R, Abee T 2013. Diversity assessment of Listeria monocytogenes biofilm formation: Impact of growth condition, serotype and strain origin. Int. J. Food Microbiol. 165:3259–64
    [Google Scholar]
  88. Kim MK, Zhao A, Wang A, Brown ZZ, Muir TW et al. 2017. Surface-attached molecules control Staphylococcus aureus quorum sensing and biofilm development. Nat. Microbiol. 2:817080
    [Google Scholar]
  89. Kim S, Bang J, Kim H, Beuchat LR, Ryu J-H 2013. Inactivation of Escherichia coli O157:H7 on stainless steel upon exposure to Paenibacillus polymyxa biofilms. Int. J. Food Microbiol. 167:3328–36
    [Google Scholar]
  90. Langsrud S, Moen B, Møretrø T, Løype M, Heir E 2016. Microbial dynamics in mixed culture biofilms of bacteria surviving sanitation of conveyor belts in salmon-processing plants. J. Appl. Microbiol. 120:2366–78
    [Google Scholar]
  91. Larsen MH, Dalmasso M, Ingmer H, Langsrud S, Malakauskas M et al. 2014. Persistence of foodborne pathogens and their control in primary and secondary food production chains. Food Control 44:92–109
    [Google Scholar]
  92. León-Romero Á, Domínguez-Manzano J, Garrido-Fernández A, Arroyo-López FN, Jiménez-Díaz R 2016. Formation of in vitro mixed-species biofilms by Lactobacillus pentosus and yeasts isolated from Spanish-style green table olive fermentations. Appl. Environ. Microbiol. 82:2689–95
    [Google Scholar]
  93. Li C, Ling F, Zhang M, Liu W-T, Li Y, Liu W 2017.a Characterization of bacterial community dynamics in a full-scale drinking water treatment plant. J. Environ. Sci. 51:21–30
    [Google Scholar]
  94. Li J, Feng J, Ma L, de la Fuente Núñez C, Gölz G, Lu X 2017.b Effects of meat juice on biofilm formation of Campylobacter and Salmonella. Int. J. Food Microbiol. 253:20–28
    [Google Scholar]
  95. Liu DZ, Jindal S, Amamcharla J, Anand S, Metzger L 2017.a Short communication: evaluation of a sol-gel-based stainless steel surface modification to reduce fouling and biofilm formation during pasteurization of milk. J. Dairy Sci. 100:42577–81
    [Google Scholar]
  96. Liu J, Prindle A, Humphries J, Gabalda-Sagarra M, Asally M et al. 2015.a Metabolic co-dependence gives rise to collective oscillations within biofilms. Nature 523:7562550–54
    [Google Scholar]
  97. Liu L, Wu R, Zhang J, Shang N, Li P 2017.b D-Ribose interferes with quorum sensing to inhibit biofilm formation of Lactobacillus paraplantarum L-ZS9. Front. Microbiol. 8:1860
    [Google Scholar]
  98. Liu NT, Lefcourt AM, Nou X, Shelton DR, Zhang G, Lo YM 2013. Native microflora in fresh-cut produce processing plants and their potentials for biofilm formation. J. Food Prot. 76:5827–32
    [Google Scholar]
  99. Liu NT, Nou X, Bauchan GR, Murphy C, Lefcourt AM et al. 2015.b Effects of environmental parameters on the dual-species biofilms formed by Escherichia coli O157:H7 and Ralstonia insidiosa, a strong biofilm producer isolated from a fresh-cut produce processing plant. J. Food Prot. 78:1121–27
    [Google Scholar]
  100. Liu NT, Nou X, Lefcourt AM, Shelton DR, Lo YM 2014. Dual-species biofilm formation by Escherichia coli O157:H7 and environmental bacteria isolated from fresh-cut processing facilities. Int. J. Food Microbiol. 171:15–20
    [Google Scholar]
  101. Liu Y, Zhang H, Wu C, Deng W, Wang D et al. 2016. Molecular analysis of dominant species in Listeria monocytogenes–positive biofilms in the drains of food processing facilities. Appl. Microbiol. Biotechnol. 100:73165–75
    [Google Scholar]
  102. Maes S, Huu SN, Heyndrickx M, van Weyenberg S, Steenackers H et al. 2017. Evaluation of two surface sampling methods for microbiological and chemical analyses to assess the presence of biofilms in food companies. J. Food Prot. 80:122022–28
    [Google Scholar]
  103. Mai-Prochnow A, Clauson M, Hong J, Murphy AB 2016. Gram positive and gram negative bacteria differ in their sensitivity to cold plasma. Sci. Rep. 6:138610
    [Google Scholar]
  104. Makovcova J, Babak V, Kulich P, Masek J, Slany M, Cincarova L 2017. Dynamics of mono- and dual-species biofilm formation and interactions between Staphylococcus aureus and gram-negative bacteria. Microb. Biotechnol. 10:4819–32
    [Google Scholar]
  105. Marco ML, Heeney D, Binda S, Cifelli CJ, Cotter PD et al. 2017. Health benefits of fermented foods: microbiota and beyond. Curr. Opin. Biotechnol. 44:94–102
    [Google Scholar]
  106. Mariani C, Oulahal N, Chamba J-F, Dubois-Brissonnet F, Notz E, Briandet R 2011. Inhibition of Listeria monocytogenes by resident biofilms present on wooden shelves used for cheese ripening. Food Control 22:81357–62
    [Google Scholar]
  107. Marin-Menguiano M, Romero-Sanchez S, Barrales RR, Ibeas JI 2017. Population analysis of biofilm yeasts during fino sherry wine aging in the Montilla-Moriles D.O. region. Int. J. Food Microbiol. 244:67–73
    [Google Scholar]
  108. Marka S, Anand S 2018. Feed substrates influence biofilm formation on reverse osmosis membranes and their cleaning efficiency. J. Dairy Sci. 101:184–95
    [Google Scholar]
  109. Marti R, Schmid M, Kulli S, Schneeberger K, Naskova J et al. 2017. Biofilm formation potential of heat-resistant Escherichia coli dairy isolates and the complete genome of multidrug-resistant, heat-resistant strain FAM21845. Appl. Environ. Microbiol. 83:15e0062817
    [Google Scholar]
  110. Martin JG, de Oliveira E, Silva G, da Fonseca CR, Morales CB, Souza Pamplona Silva C et al. 2016. Efficiency of a cleaning protocol for the removal of enterotoxigenic Staphylococcus aureus strains in dairy plants. Int. J. Food Microbiol. 238:295–301
    [Google Scholar]
  111. Mathur H, Field D, Rea MC, Cotter PD, Hill C, Ross RP 2018. Fighting biofilms with lantibiotics and other groups of bacteriocins. npj Biofilms Microbiomes 4:19
    [Google Scholar]
  112. McClean D, McNally L, Salzberg LI, Devine KM, Brown SP, Donohue I 2015. Single gene locus changes perturb complex microbial communities as much as apex predator loss. Nat. Commun. 6:18235
    [Google Scholar]
  113. McKenzie K, Maclean M, Timoshkin IV, Endarko E, MacGregor SJ, Anderson JG 2013. Photoinactivation of bacteria attached to glass and acrylic surfaces by 405 nm light: potential application for biofilm decontamination. Photochem. Photobiol. 89:4927–35
    [Google Scholar]
  114. Mo SS, Sunde M, Ilag HK, Langsrud S, Heir E 2017. Transfer potential of plasmids conferring extended-spectrum-cephalosporin resistance in Escherichia coli from poultry. Appl. Environ. Microbiol. 83:12e00654–17
    [Google Scholar]
  115. Montgomery NL, Banerjee P 2015. Inactivation of Escherichia coli O157:H7 and Listeria monocytogenes in biofilms by pulsed ultraviolet light. BMC Res. Notes 8:1235
    [Google Scholar]
  116. Moradi M, Tajik H 2017. Biofilm removal potential of neutral electrolysed water on pathogen and spoilage bacteria in dairy model systems. J. Appl. Microbiol. 123:61429–37
    [Google Scholar]
  117. Mosquera-Fernández M, Rodríguez-López P, Cabo ML, Balsa-Canto E 2014. Numerical spatio-temporal characterization of Listeria monocytogenes biofilms. Int. J. Food Microbiol. 182–183:26–36
    [Google Scholar]
  118. Nadell CD, Drescher K, Foster KR 2016. Spatial structure, cooperation and competition in biofilms. Nat. Rev. Microbiol. 14:9589–600
    [Google Scholar]
  119. Nam H, Seo H-S, Bang J, Kim H, Beuchat LR, Ryu J-H 2014. Efficacy of gaseous chlorine dioxide in inactivating Bacillus cereus spores attached to and in a biofilm on stainless steel. Int. J. Food Microbiol. 188:122–27
    [Google Scholar]
  120. Nesse LL, Sekse C, Berg K, Johannesen KCS, Solheim H et al. 2014. Potentially pathogenic Escherichia coli can form a biofilm under conditions relevant to the food production chain. Appl. Environ. Microbiol. 80:72042–49
    [Google Scholar]
  121. Nguyen UT, Burrows LL 2014. DNase I and proteinase K impair Listeria monocytogenes biofilm formation and induce dispersal of pre-existing biofilms. Int. J. Food Microbiol. 187:26–32
    [Google Scholar]
  122. Nicholas R, Dunton P, Tatham A, Fielding L 2013. The effect of ozone and open air factor on surface-attached and biofilm environmental Listeria monocytogenes. J. Appl. Microbiol. 115:2555–64
    [Google Scholar]
  123. Niemira BA, Boyd G, Sites J 2014. Cold plasma rapid decontamination of food contact surfaces contaminated with Salmonella biofilms. J. Food Sci. 79:5M917–22
    [Google Scholar]
  124. Nowak J, Cruz CD, Tempelaars M, Abee T, van Vliet AHM et al. 2017. Persistent Listeria monocytogenes strains isolated from mussel production facilities form more biofilm but are not linked to specific genetic markers. Int. J. Food Microbiol. 256:45–53
    [Google Scholar]
  125. Ochiai Y, Yamada F, Mochizuki M, Takano T, Hondo R, Ueda F 2014. Biofilm formation under different temperature conditions by a single genotype of persistent Listeria monocytogenes Strains. J. Food Prot. 77:1133–40
    [Google Scholar]
  126. Ortiz S, López V, Martínez-Suárez JV 2014. The influence of subminimal inhibitory concentrations of benzalkonium chloride on biofilm formation by Listeria monocytogenes. Int. J. Food Microbiol 189:106–12
    [Google Scholar]
  127. Overney A, Jacques-André-Coquin J, Ng P, Carpentier B, Guillier L, Firmesse O 2017. Impact of environmental factors on the culturability and viability of Listeria monocytogenes under conditions encountered in food processing plants. Int. J. Food Microbiol. 244:74–81
    [Google Scholar]
  128. Papaioannou E, Giaouris ED, Berillis P, Boziaris IS 2018. Dynamics of biofilm formation by Listeria monocytogenes on stainless steel under mono-species and mixed-culture simulated fish processing conditions and chemical disinfection challenges. Int. J. Food Microbiol. 267:9–19
    [Google Scholar]
  129. Pasvolsky R, Zakin V, Ostrova I, Shemesh M 2014. Butyric acid released during milk lipolysis triggers biofilm formation of Bacillus species. Int. J. Food Microbiol. 181:19–27
    [Google Scholar]
  130. Patel J, Singh M, Macarisin D, Sharma M, Shelton D 2013. Differences in biofilm formation of produce and poultry Salmonella enterica isolates and their persistence on spinach plants. Food Microbiol 36:2388–94
    [Google Scholar]
  131. Porru C, Rodríguez-Gómez F, Benítez-Cabello A, Jiménez-Díaz R, Zara G et al. 2018. Genotyping, identification and multifunctional features of yeasts associated to Bosana naturally black table olive fermentations. Food Microbiol 69:33–42
    [Google Scholar]
  132. Puligundla P, Mok C 2017. Potential applications of nonthermal plasmas against biofilm-associated micro-organisms in vitro. J. Appl. Microbiol. 122:51134–48
    [Google Scholar]
  133. Røder HL, Raghupathi PK, Herschend J, Brejnrod A, Knøchel S et al. 2015. Interspecies interactions result in enhanced biofilm formation by co-cultures of bacteria isolated from a food processing environment. Food Microbiol 51:18–24
    [Google Scholar]
  134. Rodríguez-López P, Saá-Ibusquiza P, Mosquera-Fernández M, López-Cabo M 2015. Listeria monocytogenes–carrying consortia in food industry. Composition, subtyping and numerical characterisation of mono-species biofilm dynamics on stainless steel. Int. J. Food Microbiol. 206:84–95
    [Google Scholar]
  135. Rosenberg G, Steinberg N, Oppenheimer-Shaanan Y, Olender T, Doron S et al. 2016. Not so simple, not so subtle: the interspecies competition between Bacillus simplex and Bacillus subtilis and its impact on the evolution of biofilms. npj Biofilms Microbiomes 2:115027
    [Google Scholar]
  136. Ruiz L, Alvarez-Ordóñez A 2016. The role of the food chain in the spread of antimicrobial resistance (AMR). Functionalized Nanomaterials for the Management of Microbial Infection R Boukherroub, S Szunerits, D Drider 23–47 Amsterdam, Neth.: Elsevier
    [Google Scholar]
  137. Sadekuzzaman M, Mizan MFR, Yang S, Kim H-S, Ha S-D 2018. Application of bacteriophages for the inactivation of Salmonella spp. in biofilms. Food Sci. Technol. Int. 24:5424–33
    [Google Scholar]
  138. Sadekuzzaman M, Yang S, Mizan MFR, Ha S-D 2017. Reduction of Escherichia coli O157:H7 in biofilms using bacteriophage BPECO 19. J. Food Sci. 82:61433–42
    [Google Scholar]
  139. Sadiq FA, Flint S, Yuan L, Li Y, Liu T, He G 2017. Propensity for biofilm formation by aerobic mesophilic and thermophilic spore forming bacteria isolated from Chinese milk powders. Int. J. Food Microbiol. 262:89–98
    [Google Scholar]
  140. Sanchez-Vizuete P, Orgaz B, Aymerich S, Le Coq D, Briandet R 2015. Pathogens protection against the action of disinfectants in multispecies biofilms. Front. Microbiol. 6:705
    [Google Scholar]
  141. Scatassa ML, Gaglio R, Macaluso G, Francesca N, Randazzo W et al. 2015. Transfer, composition and technological characterization of the lactic acid bacterial populations of the wooden vats used to produce traditional stretched cheeses. Food Microbiol 52:31–41
    [Google Scholar]
  142. Schlisselberg DB, Yaron S 2013. The effects of stainless steel finish on Salmonella Typhimurium attachment, biofilm formation and sensitivity to chlorine. Food Microbiol 35:165–72
    [Google Scholar]
  143. Seghal Kiran G, Nishanth Lipton A, Kennedy J, Dobson AD, Selvin J 2014. A halotolerant thermostable lipase from the marine bacterium Oceanobacillus sp. PUMB02 with an ability to disrupt bacterial biofilms. Bioengineered 5:5305–18
    [Google Scholar]
  144. Sepehr S, Rahmani-Badi A, Babaie-Naiej H, Soudi MR 2014. Unsaturated fatty acid, cis-2-decenoic acid, in combination with disinfectants or antibiotics removes pre-established biofilms formed by food-related bacteria. PLOS ONE 9:7e101677
    [Google Scholar]
  145. Shafique M, Alvi IA, Abbas Z, ur Rehman S 2017. Assessment of biofilm removal capacity of a broad host range bacteriophage JHP against Pseudomonas aeruginosa. APMIS 125:6579–84
    [Google Scholar]
  146. Shemesh M, Pasvolsky R, Zakin V 2014. External pH is a cue for the behavioral switch that determines surface motility and biofilm formation of Alicyclobacillus acidoterrestris. J. Food Prot. 77:81418–23
    [Google Scholar]
  147. Skovager A, Larsen MH, Castro-Mejia JL, Hecker M, Albrecht D et al. 2013. Initial adhesion of Listeria monocytogenes to fine polished stainless steel under flow conditions is determined by prior growth conditions. Int. J. Food Microbiol. 165:135–42
    [Google Scholar]
  148. Slany M, Oppelt J, Cincarova L 2017. Formation of Staphylococcus aureus biofilm in the presence of sublethal concentrations of disinfectants studied via a transcriptomic analysis using transcriptome sequencing (RNA-seq). Appl. Environ. Microbiol. 83:24e01643–17
    [Google Scholar]
  149. Somerton B, Lindsay D, Palmer J, Brooks J, Flint S 2015. Changes in sodium, calcium, and magnesium ion concentrations that inhibit geobacillus biofilms have no effect on Anoxybacillus flavithermus biofilms. Appl. Environ. Microbiol. 81:155115–22
    [Google Scholar]
  150. Son H, Park S, Beuchat LR, Kim H, Ryu J-H 2016. Inhibition of Staphylococcus aureus by antimicrobial biofilms formed by competitive exclusion microorganisms on stainless steel. Int. J. Food Microbiol. 238:165–71
    [Google Scholar]
  151. Stevens MRE, Luo TL, Vornhagen J, Jakubovics NS, Gilsdorf JR et al. 2015. Coaggregation occurs between microorganisms isolated from different environments. FEMS Microbiol. Ecol. 91:11fiv123
    [Google Scholar]
  152. Strathmann M, Mittenzwey K-H, Sinn G, Papadakis W, Flemming H-C 2013. Simultaneous monitoring of biofilm growth, microbial activity, and inorganic deposits on surfaces with an in situ, online, real-time, non-destructive, optical sensor. Biofouling 29:5573–83
    [Google Scholar]
  153. Tack ILMM, Nimmegeers P, Akkermans S, Hashem I, Van Impe JFM 2017. Simulation of Escherichia coli dynamics in biofilms and submerged colonies with an individual-based model including metabolic network information. Front. Microbiol. 8:2509
    [Google Scholar]
  154. Tarifa MC, Genovese D, Lozano JE, Brugnoni LI 2017. In situ microstructure and rheological behavior of yeast biofilms from the juice processing industries. Biofouling 34:74–85
    [Google Scholar]
  155. Techaruvichit P, Takahashi H, Kuda T, Miya S, Keeratipibul S, Kimura B 2016. Adaptation of Campylobacter jejuni to biocides used in the food industry affects biofilm structure, adhesion strength, and cross-resistance to clinical antimicrobial compounds. Biofouling 32:7827–39
    [Google Scholar]
  156. Thiran E, Di Ciccio PA, Graber HU, Zanardi E, Ianieri A, Hummerjohann J 2017. Biofilm formation of Staphylococcus aureus dairy isolates representing different genotypes. J. Dairy Sci. 101:21000–12
    [Google Scholar]
  157. Turonova H, Briandet R, Rodrigues R, Hernould M, Hayek N et al. 2015. Biofilm spatial organization by the emerging pathogen Campylobacter jejuni: comparison between NCTC 11168 and 81–176 strains under microaerobic and oxygen-enriched conditions. Front. Microbiol. 6:709
    [Google Scholar]
  158. Valderrama WB, Ostiguy N, Cutter CN 2014. Multivariate analysis reveals differences in biofilm formation capacity among Listeria monocytogenes lineages. Biofouling 30:101199–209
    [Google Scholar]
  159. Van Meervenne E, De Weirdt R, Van Coillie E, Devlieghere F, Herman L, Boon N 2014. Biofilm models for the food industry: hot spots for plasmid transfer?. Pathog. Dis. 70:3332–38
    [Google Scholar]
  160. Visvalingam J, Ells TC, Yang X 2017. Impact of persistent and nonpersistent generic Escherichia coli and Salmonella sp. recovered from a beef packing plant on biofilm formation by E. coli O157. J. Appl. Microbiol. 123:61512–21
    [Google Scholar]
  161. Vogeleer P, Tremblay YDN, Jubelin G, Jacques M, Harel J 2016. Biofilm-forming abilities of Shiga toxin–producing Escherichia coli isolates associated with human infections. Appl. Environ. Microbiol. 82:51448–58
    [Google Scholar]
  162. Wang J, Ray AJ, Hammons SR, Oliver HF 2015.a Persistent and transient Listeria monocytogenes strains from retail deli environments vary in their ability to adhere and form biofilms and rarely have inlA premature stop codons. Foodborne Pathog. Dis. 12:2151–58
    [Google Scholar]
  163. Wang R, Kalchayanand N, Bono JL 2015.b Sequence of colonization determines the composition of mixed biofilms by Escherichia coli O157:H7 and O111:H8 strains. J. Food Prot. 78:81554–59
    [Google Scholar]
  164. Wang R, Kalchayanand N, Schmidt JW, Harhay DM 2013. Mixed biofilm formation by Shiga toxin–producing Escherichia coli and Salmonella enterica serovar Typhimurium enhanced bacterial resistance to sanitization due to extracellular polymeric substances. J. Food Prot. 76:91513–22
    [Google Scholar]
  165. Wang R, Luedtke BE, Bosilevac JM, Schmidt JW, Kalchayanand N, Arthur TM 2016. Escherichia coli O157:H7 strains isolated from high-event period beef contamination have strong biofilm-forming ability and low sanitizer susceptibility, which are associated with high pO157 plasmid copy number. J. Food Prot. 79:111875–83
    [Google Scholar]
  166. Weiler C, Ifland A, Naumann A, Kleta S, Noll M 2013. Incorporation of Listeria monocytogenes strains in raw milk biofilms. Int. J. Food Microbiol. 161:261–68
    [Google Scholar]
  167. Xue T, Chen X, Shang F 2014. Short communication: effects of lactose and milk on the expression of biofilm-associated genes in Staphylococcus aureus strains isolated from a dairy cow with mastitis. J. Dairy Sci. 97:106129–34
    [Google Scholar]
  168. Yu S, Su T, Wu H, Liu S, Wang D et al. 2015. PslG, a self-produced glycosyl hydrolase, triggers biofilm disassembly by disrupting exopolysaccharide matrix. Cell Res 25:121352–67
    [Google Scholar]
  169. Zetzmann M, Okshevsky M, Endres J, Sedlag A, Caccia N et al. 2015. DNase-sensitive and -resistant modes of biofilm formation by Listeria monocytogenes. Front. Microbiol 6:1428
    [Google Scholar]
  170. Zhao T, Podtburg TC, Zhao P, Chen D, Baker DA et al. 2013.a Reduction by competitive bacteria of Listeria monocytogenes in biofilms and Listeria bacteria in floor drains in a ready-to-eat poultry processing plant. J. Food Prot. 76:4601–7
    [Google Scholar]
  171. Zhao Y, Caspers MPM, Metselaar KI, de Boer P, Roeselers G et al. 2013.b Abiotic and microbiotic factors controlling biofilm formation by thermophilic sporeformers. Appl. Environ. Microbiol. 79:185652–60
    [Google Scholar]
  172. Ziuzina D, Boehm D, Patil S, Cullen PJ, Bourke P 2015.a Cold plasma inactivation of bacterial biofilms and reduction of quorum sensing regulated virulence factors. PLOS ONE 10:9e0138209
    [Google Scholar]
  173. Ziuzina D, Han L, Cullen PJ, Bourke P 2015.b Cold plasma inactivation of internalised bacteria and biofilms for Salmonella enterica serovar Typhimurium, Listeria monocytogenes and Escherichia coli. Int. J. Food Microbiol. 210:53–61
    [Google Scholar]
/content/journals/10.1146/annurev-food-032818-121805
Loading
/content/journals/10.1146/annurev-food-032818-121805
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error